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Isolation and Characterization of Microsatellite Markers in Garcinia Gummi-Gutta by Next-Generation Sequencing and Cross-Species Amplification

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Isolation and Characterization of Microsatellite Markers in Garcinia Gummi-Gutta by Next-Generation Sequencing and Cross-Species Amplification c Indian Academy of Sciences RESEARCH ARTICLE Isolation and characterization of microsatellite markers in Garcinia gummi-gutta by next-generation sequencing and cross-species amplification K. V. RAVISHANKAR1∗, R. VASUDEVA2, BYATROY HEMANTH1, B. S. SANDYA1,B.R.STHAPIT3, V. A. PARTHASARATHY1 and V. RAMANATHA RAO4 1ICAR-Indian Institute of Horticultural Research, Bengaluru 560 089, India 2Department of Forest Biology and Tree Improvement, College of Forestry Sirsi, University of Agricultural Sciences, Dharwad 581 401, India 3Biodiversity International, 93.4, Dharhara Marg, Fulbari, Ward no.11, Pokhara, Nepal 4Bioversity International, University of Horticultural Sciences, GKVK, Bengaluru 560 065, India Abstract Garcinia gummi-gutta (L.) Roxb. (Clusiaceae) is an endemic, semidomesticated, fruit-yielding tree species distributed in the Western Ghats of India and Sri Lanka. Various bioactive phytochemicals, such as garcinol, benzophenones and xanthones are isolated from G. gummi-gutta and have shown antibacterial, antiviral and antioxidant activities. We sequenced the total genomic DNA using Illumina Hiseq 2000 platform and examined 241,141,804 bp high quality data, assembled into 773,889 contigs. In these contigs, 27,313 simple-sequence repeats (SSRs) were identified, among which mononucleotide repeats were predominant (44.98%) followed by dinucleotide and trinucleotide repeats. Primers were designed for 9964 microsatellites among which 32 randomly selected SSR primer pairs were standardized for amplification. Polymerase chain reaction (PCR) amplification of genomic DNA in 30 G. gummi-gutta genotypes revealed polymorphic information content (PIC) across all 32 loci ranging from 0.867 to 0.951, with a mean value of 0.917. The observed and expected heterozygosity ranged from 0.00 to 0.63 and 0.896 to 0.974, respectively. Alleles per locus ranged from 12 to 27. This is the first report on the development of genomic SSR markers in G. gummi-gutta using next-generation sequencing technology. The genomic SSR markers developed in this study will be useful in identification, mapping, diversity and breeding studies. [Ravishankar K. V., Vasudeva R., Hemanth B., Sandya B. S., Sthapit B. R., Parthasarathy V. A. and Rao V. R. 2017 Isolation and charac- terization of microsatellite markers in Garcinia gummi-gutta by next-generation sequencing and cross-species amplification. J. Genet. 96, 213–218] Introduction rind of the uppage fruit has been traditionally used in India and Sri Lanka as a culinary additive and fish preserva- Garcinia gummi-gutta (L.) Roxb., popularly known as ‘Mal- tive (Samarajeewa and Shanmugapirabu 1983; Bhagyavanth abar Gamboge’ (in English) ‘uppage’ (in Kannada) belongs et al. 2010). Many studies showed that hydroxycitric acid to the family Clusiaceae. It is a moderate-sized dioecious (HCA), a secondary compound present in the rind of uppage tree with round canopy, drooping branches and smooth dark fruit is effective in weight loss (Jena et al. 2002). The barks. It is common in lower Shola forests of the West- ern Ghats, India, up to an altitude of 1800 mean sea level. extract obtained from this fruits has exhibited the property of G. gummi-gutta is recognized in Ayurveda, the traditional antiobesity. Recently, a number of studies have shown that Indian system of medicine, for better digestion and is pre- G. gummi-gutta fruit extracts are rich in HCA and are effec- scribed against abdominal disorders and heart diseases. The tive in reducing body weight (Shara et al. 2004; Saito et al. fruit rind is ground and used as a sour flavouring spice in 2005). the preparation of curries and to garnish fish preparations. The Germplasm utilization and conservation requires precise information on the genetics, genetic relationships and diver- ∗ For correspondence. E-mail: [email protected]; sity. Earlier, a few studies attempted to examine diversity [email protected]. using random amplified polymorphic DNA (RAPD) and Keywords. microsatellite markers; cross-species amplification; next-generation sequencing; Garcinia gummi-gutta. Journal of Genetics, DOI 10.1007/s12041-017-0756-0, Vol. 96, No. 2, June 2017 213 K. V. Ravishankar et al. inter-simple sequence repeat (ISSR) markers (Mohan et al. PCR and genotyping 2012; Parthasarathy et al. 2013). However, development of We selected 50 SSR primer sets randomly and synthe- microsatellite markers have helped in fingerprinting unique sized with M13 tail. These M13 tailed primers were trees, assessing degree of diversity in the populations, and first screened for amplification using pooled total genomic identifying marker tightly linked to the important agronomic DNA from five randomly selected genotypes. We used traits like active ingredients, and resistance to biotic and fluorescence-based M13 tailing PCR method following abiotic stresses. Therefore, the development of markers has Schuelke (2000) to amplify the microsatellites in a quick, become a prerequisite for genetic studies (Bohra et al. 2011; accurate and efficient manner. The forward primer tailed Dutta et al. 2011). Keeping this in view, here, we report the with 5 -GTAAAACGACGGCCAGT-3 and reverse primer development and standardization of microsatellite markers tailed with 5 -GTTTCTT-3 . PCR was carried out in 20 μL of G. gummi-gutta using next-generation sequencing (NGS) reaction volume containing 2 μLof10× reaction buffer, and their cross species transferability. 2.0 μL of 1 mM dNTPs, 0.9 μL (5 pmol) of forward, 0.9 μL reverse primers (5 pmol), labelled M13 probes (HEX, NED, Materials and methods VIC, TET) 1.2 μL(5pmol),5.0μL (50–75 ng) of tem- plate genomic DNA, 0.8 μL(2U)ofTaq DNA polymerase Plant materials and 7.2 μL of nuclease free water. The PCR cycling profile The total genomic DNA from G. gummi-gutta was used for was: initial denaturation at 94◦C for 2 min, followed by 35 genome sequencing. We have also included Garcinia indica cycles of 94◦C for 30 s, 55◦C for 30 s, 72◦Cfor1minanda and Garcinia morella to examine cross species transferabil- final extension at 72◦C for 5 min. PCR reaction was carried ity of isolated microsatellite markers. The leaf material was out using thermocycler (Eppendrof Master Cycler Gradient, obtained from the germplasm collection of the College of Germany). Amplified products were initially separated on Forestry, Sirsi (University of Agricultural Sciences, Dhar- 3% agarose gel to confirm the amplification. Finally, 32 SSR wad), India (see details in table 1 in electronic supplementary primers were selected based on amplification of clear PCR material at http://www.ias.ac.in/jgenet/). The leaf samples products. These primers were employed for amplification of ◦ were obtained from Jaddi Gadde collection (14 44 13.2 N 30 genotypes of G. gummi-gutta and one genotype each of ◦ latitude and 74 43 03.2 E longitude with altitude of 498 m). G. indica and G. morella. The PCR products were separated The authenticated herbarium specimens were deposited to using automated DNA Sequencer (Applied Biosystems, ABI the herbarium of College of Forestry, Department of Forest 3730 DNA Analyzer) through capillary electrophoresis, at Biology and Tree improvement. M/S Eurofins facility, Bengaluru. Genome sequencing and assembly Genetic analysis of SSR markers High-quality genomic DNA was isolated from the leaves of 30 G. gummi-gutta genotypes, one genotype from each of G. The raw data generated was analysed and compiled using indica and G. morella (table 1 in electronic supplementary Peak Scanner ver. 1.0 software (Applied Biosystems, Foster material) following modified CTAB method (Ravishankar Table 1. Details of sequenced genomic data. et al. 2000). Total genomic DNA was sequenced using NGS Illumina HiSeq2000 platform at M/s Genotypic Bengaluru Sequencing details facility following manufactures instructions. High-quality sequence reads (Q > 20; >70% bases in a read) were used Total number of contigs 773889 for de novo assembly into contigs using SOAPdenovo2 soft- Total number of examined sequences (bp) 241141804 Total number of identified SSRs 27313 ware (Luo et al. 2012). Assembly with Kmer-63 was selected Number of SSR containing contigs 26663 as it has the optimal readings for N50. Number of SSR containing more than one SSR 631 Survey, identification and design primers for genomic Table 2. Simple-sequence repeat types in the G. gummi-gutta microsatellite markers contigs sequences. The Perl Script software program MISA (http://pgrc.ipk- gatersleben.de/misa/)(Thielet al. 2003; Ravishankar et al. 2015) Motif length Number of SSR Frequency (%) was used for identification of SSRs from assembled con- Mononucleotide 12286 44.98 tigs (Feng et al. 2009; Ravishankar et al. 2015). MISA Dinucleotide 9638 35.29 files were transferred to Microsoft Excel where SSRs were Trinucleotide 3003 10.99 classified into mononucleotide, dinucleotide, trinucleotide, Tetranucleotide 552 2.02 tetranucleotide, pentanucleotide and hexanucleotide repeats Pentanucleotide 249 0.91 and compound repeats. Primer pairs flanking the repeats Hexanucleotide 58 0.21 Complex/compound 1527 5.59 were designed using Primer3 software (Untergrasser et al. Total 27313 2012)(table2 in electronic supplementary material). 214 Journal of Genetics, Vol. 96, No. 2, June 2017 Table 3. Genetic analysis of microsatellite markers developed for G. gummi-gutta. Number Observed Observed Expected Polymorphic Probability Cross species Repeat of allele size range heterozygosity heterozygosity information of identity amplification Locus name Forward sequence 5 → 3 Reverse sequence 5 → 3
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